Abstract

In this paper, we present an automated approach to quantify information about three-dimensional (3D) morphology, hemoglobin content and density of mature red blood cells (RBCs) using off-axis digital holographic microscopy (DHM) and statistical algorithms. The digital hologram of RBCs is recorded by a CCD camera using an off-axis interferometry setup and quantitative phase images of RBCs are obtained by a numerical reconstruction algorithm. In order to remove unnecessary parts and obtain clear targets in the reconstructed phase image with many RBCs, the marker-controlled watershed segmentation algorithm is applied to the phase image. Each RBC in the segmented phase image is three-dimensionally investigated. Characteristic properties such as projected cell surface, average phase, sphericity coefficient, mean corpuscular hemoglobin (MCH) and MCH surface density of each RBC is quantitatively measured. We experimentally demonstrate that joint statistical distributions of the characteristic parameters of RBCs can be obtained by our algorithm and efficiently used as a feature pattern to discriminate between RBC populations that differ in shape and hemoglobin content. Our study opens the possibility of automated RBC quantitative analysis suitable for the rapid classification of a large number of RBCs from an individual blood specimen, which is a fundamental step to develop a diagnostic approach based on DHM.

© 2012 OSA

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2011

2010

2009

V. Micó, J. García, Z. Zalevsky, and B. Javidi, “Phase-shifting Gabor holography,” Opt. Lett. 34(10), 1492–1494 (2009).
[CrossRef] [PubMed]

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt. 14(1), 014018 (2009).
[CrossRef] [PubMed]

B. Rappaz, E. Cano, T. Colomb, J. Kühn, C. Depeursinge, V. Simanis, P. J. Magistretti, and P. Marquet, “Noninvasive characterization of the fission yeast cell cycle by monitoring dry mass with digital holographic microscopy,” J. Biomed. Opt. 14(3), 034049 (2009).
[CrossRef] [PubMed]

2008

L. Martínez-León and B. Javidi, “Synthetic aperture single-exposure on-axis digital holography,” Opt. Express 16(1), 161–169 (2008).
[CrossRef] [PubMed]

B. Rappaz, A. Barbul, Y. Emery, R. Korenstein, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Comparative study of human erythrocytes by digital holographic microscopy, confocal microscopy, and impedance volume analyzer,” Cytometry A 73A(10), 895–903 (2008).
[CrossRef] [PubMed]

2007

2006

2005

2004

2002

H. W. G. Lim, M. Wortis, and R. Mukhopadhyay, “Stomatocyte-discocyte-echinocyte sequence of the human red blood cell: evidence for the bilayer- couple hypothesis from membrane mechanics,” Proc. Natl. Acad. Sci. U.S.A. 99(26), 16766–16769 (2002).
[CrossRef] [PubMed]

U. Schnars and W. P. O. Jueptner, “Digital recording and numerical reconstruction of holograms,” Meas. Sci. Technol. 13(9), R85–R101 (2002).
[CrossRef]

2000

1999

1967

J. W. Goodman and R. W. Lawrence, “Digital image formation from electronically detected holograms,” Appl. Phys. Lett. 11(3), 77–79 (1967).
[CrossRef]

1952

R. Barer, “Interference microscopy and mass determination,” Nature 169(4296), 366–367 (1952).
[CrossRef] [PubMed]

Alfieri, D.

Aspert, N.

Barbul, A.

B. Rappaz, A. Barbul, Y. Emery, R. Korenstein, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Comparative study of human erythrocytes by digital holographic microscopy, confocal microscopy, and impedance volume analyzer,” Cytometry A 73A(10), 895–903 (2008).
[CrossRef] [PubMed]

Barer, R.

R. Barer, “Interference microscopy and mass determination,” Nature 169(4296), 366–367 (1952).
[CrossRef] [PubMed]

Bernhardt, I.

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt. 14(1), 014018 (2009).
[CrossRef] [PubMed]

Cano, E.

B. Rappaz, E. Cano, T. Colomb, J. Kühn, C. Depeursinge, V. Simanis, P. J. Magistretti, and P. Marquet, “Noninvasive characterization of the fission yeast cell cycle by monitoring dry mass with digital holographic microscopy,” J. Biomed. Opt. 14(3), 034049 (2009).
[CrossRef] [PubMed]

Carapezza, E.

Charrière, F.

Colomb, T.

Coppola, G.

Costescu, J.

Cuche, E.

De Nicola, S.

Depeursinge, C.

B. Rappaz, E. Cano, T. Colomb, J. Kühn, C. Depeursinge, V. Simanis, P. J. Magistretti, and P. Marquet, “Noninvasive characterization of the fission yeast cell cycle by monitoring dry mass with digital holographic microscopy,” J. Biomed. Opt. 14(3), 034049 (2009).
[CrossRef] [PubMed]

B. Rappaz, A. Barbul, Y. Emery, R. Korenstein, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Comparative study of human erythrocytes by digital holographic microscopy, confocal microscopy, and impedance volume analyzer,” Cytometry A 73A(10), 895–903 (2008).
[CrossRef] [PubMed]

T. Colomb, E. Cuche, F. Charrière, J. Kühn, N. Aspert, F. Montfort, P. Marquet, and C. Depeursinge, “Automatic procedure for aberration compensation in digital holographic microscopy and applications to specimen shape compensation,” Appl. Opt. 45(5), 851–863 (2006).
[CrossRef] [PubMed]

P. Marquet, B. Rappaz, E. Cuche, T. Colomb, Y. Emery, C. Depeursinge, and P. Magistretti, “Digital holographic microscopy: a noninvasive contrast imaging technique allowing quantitative visualization of living cells with subwavelength axial accuracy,” Opt. Lett. 30, 468–470 (2005).
[CrossRef] [PubMed]

E. Cuche, P. Marquet, and C. Depeursinge, “Spatial filtering for zero-order and twin-image elimination in digital off-axis holography,” Appl. Opt. 39(23), 4070–4075 (2000).
[CrossRef] [PubMed]

E. Cuche, P. Marquet, and C. Depeursinge, “Simultaneous amplitude and quantitative phase contrast microscopy by numerical reconstruction of Fresnel off-axis holograms,” Appl. Opt. 38(34), 6994–7001 (1999).
[CrossRef] [PubMed]

Dirksen, D.

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt. 14(1), 014018 (2009).
[CrossRef] [PubMed]

Dubois, F.

Eigenthaler, U.

Emery, Y.

B. Rappaz, A. Barbul, Y. Emery, R. Korenstein, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Comparative study of human erythrocytes by digital holographic microscopy, confocal microscopy, and impedance volume analyzer,” Cytometry A 73A(10), 895–903 (2008).
[CrossRef] [PubMed]

P. Marquet, B. Rappaz, E. Cuche, T. Colomb, Y. Emery, C. Depeursinge, and P. Magistretti, “Digital holographic microscopy: a noninvasive contrast imaging technique allowing quantitative visualization of living cells with subwavelength axial accuracy,” Opt. Lett. 30, 468–470 (2005).
[CrossRef] [PubMed]

Faridian, A.

Ferraro, P.

Finizio, A.

Frauel, Y.

Y. Frauel, T. J. Naughton, O. Matoba, E. Tajahuerce, and B. Javidi, “Three dimensional imaging and display using computational holographic imaging,” Proc. IEEE 94(3), 636–653 (2006).
[CrossRef]

García, J.

Georgiev, G.

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt. 14(1), 014018 (2009).
[CrossRef] [PubMed]

Gheorghiu, A.

Goodman, J. W.

J. W. Goodman and R. W. Lawrence, “Digital image formation from electronically detected holograms,” Appl. Phys. Lett. 11(3), 77–79 (1967).
[CrossRef]

Grilli, S.

Hirscher, M.

Hopp, D.

Ivanova, L.

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt. 14(1), 014018 (2009).
[CrossRef] [PubMed]

Javidi, B.

V. Micó, J. García, Z. Zalevsky, and B. Javidi, “Phase-shifting Gabor holography,” Opt. Lett. 34(10), 1492–1494 (2009).
[CrossRef] [PubMed]

L. Martínez-León and B. Javidi, “Synthetic aperture single-exposure on-axis digital holography,” Opt. Express 16(1), 161–169 (2008).
[CrossRef] [PubMed]

T. Nomura, B. Javidi, S. Murata, E. Nitanai, and T. Numata, “Polarization imaging of a 3D object by use of on-axis phase-shifting digital holography,” Opt. Lett. 32(5), 481–483 (2007).
[CrossRef] [PubMed]

A. Stern and B. Javidi, “Theoretical analysis of three-dimensional imaging and recognition of micro-organisms with a single-exposure on-line holographic microscope,” J. Opt. Soc. Am. A 24, 163–168 (2007).
[CrossRef]

I. Moon and B. Javidi, “Three-dimensional identification of stem cells by computational holographic imaging,” J. R. Soc. Interface 4, 305–313 (2007).
[CrossRef] [PubMed]

Y. Frauel, T. J. Naughton, O. Matoba, E. Tajahuerce, and B. Javidi, “Three dimensional imaging and display using computational holographic imaging,” Proc. IEEE 94(3), 636–653 (2006).
[CrossRef]

P. Ferraro, S. Grilli, D. Alfieri, S. De Nicola, A. Finizio, G. Pierattini, B. Javidi, G. Coppola, and V. Striano, “Extended focused image in microscopy by digital Holography,” Opt. Express 13(18), 6738–6749 (2005).
[CrossRef] [PubMed]

B. Javidi, I. Moon, S. Yeom, and E. Carapezza, “Three-dimensional imaging and recognition of microorganism using single-exposure on-line (SEOL) digital holography,” Opt. Express 13(12), 4492–4506 (2005).
[CrossRef] [PubMed]

B. Javidi and E. Tajahuerce, “Three-dimensional object recognition by use of digital holography,” Opt. Lett. 25(9), 610–612 (2000).
[CrossRef] [PubMed]

Joannes, L.

Jueptner, W. P. O.

U. Schnars and W. P. O. Jueptner, “Digital recording and numerical reconstruction of holograms,” Meas. Sci. Technol. 13(9), R85–R101 (2002).
[CrossRef]

Kemper, B.

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt. 14(1), 014018 (2009).
[CrossRef] [PubMed]

Ketelhut, S.

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt. 14(1), 014018 (2009).
[CrossRef] [PubMed]

Korenstein, R.

B. Rappaz, A. Barbul, Y. Emery, R. Korenstein, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Comparative study of human erythrocytes by digital holographic microscopy, confocal microscopy, and impedance volume analyzer,” Cytometry A 73A(10), 895–903 (2008).
[CrossRef] [PubMed]

Kühn, J.

B. Rappaz, E. Cano, T. Colomb, J. Kühn, C. Depeursinge, V. Simanis, P. J. Magistretti, and P. Marquet, “Noninvasive characterization of the fission yeast cell cycle by monitoring dry mass with digital holographic microscopy,” J. Biomed. Opt. 14(3), 034049 (2009).
[CrossRef] [PubMed]

T. Colomb, E. Cuche, F. Charrière, J. Kühn, N. Aspert, F. Montfort, P. Marquet, and C. Depeursinge, “Automatic procedure for aberration compensation in digital holographic microscopy and applications to specimen shape compensation,” Appl. Opt. 45(5), 851–863 (2006).
[CrossRef] [PubMed]

Kusko, M.

Langehanenberg, P.

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt. 14(1), 014018 (2009).
[CrossRef] [PubMed]

Lawrence, R. W.

J. W. Goodman and R. W. Lawrence, “Digital image formation from electronically detected holograms,” Appl. Phys. Lett. 11(3), 77–79 (1967).
[CrossRef]

Legros, J.-C.

Lim, H. W. G.

H. W. G. Lim, M. Wortis, and R. Mukhopadhyay, “Stomatocyte-discocyte-echinocyte sequence of the human red blood cell: evidence for the bilayer- couple hypothesis from membrane mechanics,” Proc. Natl. Acad. Sci. U.S.A. 99(26), 16766–16769 (2002).
[CrossRef] [PubMed]

Magistretti, P.

Magistretti, P. J.

B. Rappaz, E. Cano, T. Colomb, J. Kühn, C. Depeursinge, V. Simanis, P. J. Magistretti, and P. Marquet, “Noninvasive characterization of the fission yeast cell cycle by monitoring dry mass with digital holographic microscopy,” J. Biomed. Opt. 14(3), 034049 (2009).
[CrossRef] [PubMed]

B. Rappaz, A. Barbul, Y. Emery, R. Korenstein, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Comparative study of human erythrocytes by digital holographic microscopy, confocal microscopy, and impedance volume analyzer,” Cytometry A 73A(10), 895–903 (2008).
[CrossRef] [PubMed]

Mahalanobis, A.

Marquet, P.

B. Rappaz, E. Cano, T. Colomb, J. Kühn, C. Depeursinge, V. Simanis, P. J. Magistretti, and P. Marquet, “Noninvasive characterization of the fission yeast cell cycle by monitoring dry mass with digital holographic microscopy,” J. Biomed. Opt. 14(3), 034049 (2009).
[CrossRef] [PubMed]

B. Rappaz, A. Barbul, Y. Emery, R. Korenstein, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Comparative study of human erythrocytes by digital holographic microscopy, confocal microscopy, and impedance volume analyzer,” Cytometry A 73A(10), 895–903 (2008).
[CrossRef] [PubMed]

T. Colomb, E. Cuche, F. Charrière, J. Kühn, N. Aspert, F. Montfort, P. Marquet, and C. Depeursinge, “Automatic procedure for aberration compensation in digital holographic microscopy and applications to specimen shape compensation,” Appl. Opt. 45(5), 851–863 (2006).
[CrossRef] [PubMed]

P. Marquet, B. Rappaz, E. Cuche, T. Colomb, Y. Emery, C. Depeursinge, and P. Magistretti, “Digital holographic microscopy: a noninvasive contrast imaging technique allowing quantitative visualization of living cells with subwavelength axial accuracy,” Opt. Lett. 30, 468–470 (2005).
[CrossRef] [PubMed]

E. Cuche, P. Marquet, and C. Depeursinge, “Spatial filtering for zero-order and twin-image elimination in digital off-axis holography,” Appl. Opt. 39(23), 4070–4075 (2000).
[CrossRef] [PubMed]

E. Cuche, P. Marquet, and C. Depeursinge, “Simultaneous amplitude and quantitative phase contrast microscopy by numerical reconstruction of Fresnel off-axis holograms,” Appl. Opt. 38(34), 6994–7001 (1999).
[CrossRef] [PubMed]

Martínez-León, L.

Matoba, O.

Y. Frauel, T. J. Naughton, O. Matoba, E. Tajahuerce, and B. Javidi, “Three dimensional imaging and display using computational holographic imaging,” Proc. IEEE 94(3), 636–653 (2006).
[CrossRef]

Micó, V.

Mihailescu, M.

Montfort, F.

Moon, I.

Mukhopadhyay, R.

H. W. G. Lim, M. Wortis, and R. Mukhopadhyay, “Stomatocyte-discocyte-echinocyte sequence of the human red blood cell: evidence for the bilayer- couple hypothesis from membrane mechanics,” Proc. Natl. Acad. Sci. U.S.A. 99(26), 16766–16769 (2002).
[CrossRef] [PubMed]

Murata, S.

Naughton, T. J.

Y. Frauel, T. J. Naughton, O. Matoba, E. Tajahuerce, and B. Javidi, “Three dimensional imaging and display using computational holographic imaging,” Proc. IEEE 94(3), 636–653 (2006).
[CrossRef]

Nitanai, E.

Nomura, T.

Numata, T.

Osten, W.

Paun, I. A.

Pedrini, G.

Pierattini, G.

Rappaz, B.

B. Rappaz, E. Cano, T. Colomb, J. Kühn, C. Depeursinge, V. Simanis, P. J. Magistretti, and P. Marquet, “Noninvasive characterization of the fission yeast cell cycle by monitoring dry mass with digital holographic microscopy,” J. Biomed. Opt. 14(3), 034049 (2009).
[CrossRef] [PubMed]

B. Rappaz, A. Barbul, Y. Emery, R. Korenstein, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Comparative study of human erythrocytes by digital holographic microscopy, confocal microscopy, and impedance volume analyzer,” Cytometry A 73A(10), 895–903 (2008).
[CrossRef] [PubMed]

P. Marquet, B. Rappaz, E. Cuche, T. Colomb, Y. Emery, C. Depeursinge, and P. Magistretti, “Digital holographic microscopy: a noninvasive contrast imaging technique allowing quantitative visualization of living cells with subwavelength axial accuracy,” Opt. Lett. 30, 468–470 (2005).
[CrossRef] [PubMed]

Sadjadi, F. A.

Scarlat, E.

Scarlat, M.

Schnars, U.

U. Schnars and W. P. O. Jueptner, “Digital recording and numerical reconstruction of holograms,” Meas. Sci. Technol. 13(9), R85–R101 (2002).
[CrossRef]

Simanis, V.

B. Rappaz, E. Cano, T. Colomb, J. Kühn, C. Depeursinge, V. Simanis, P. J. Magistretti, and P. Marquet, “Noninvasive characterization of the fission yeast cell cycle by monitoring dry mass with digital holographic microscopy,” J. Biomed. Opt. 14(3), 034049 (2009).
[CrossRef] [PubMed]

Stern, A.

Striano, V.

Tajahuerce, E.

Y. Frauel, T. J. Naughton, O. Matoba, E. Tajahuerce, and B. Javidi, “Three dimensional imaging and display using computational holographic imaging,” Proc. IEEE 94(3), 636–653 (2006).
[CrossRef]

B. Javidi and E. Tajahuerce, “Three-dimensional object recognition by use of digital holography,” Opt. Lett. 25(9), 610–612 (2000).
[CrossRef] [PubMed]

Tiziani, H. J.

Vollmer, A.

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt. 14(1), 014018 (2009).
[CrossRef] [PubMed]

von Bally, G.

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Figures (11)

Fig. 1
Fig. 1

Schematic of the off-axis digital holographic microscopy used in the experiments

Fig. 2
Fig. 2

The sphericity coefficient k is defined as a ratio of two quantities (phc, phd) in the RBC. The phc and phd are phase values at the center of RBC and quarter of its diameter, respectively. d is the diameter of RBC.

Fig. 3
Fig. 3

The reconstructed red blood cells phase images: (a) The red blood cells (RBCs) on day 14 with predominantly stomatocyte shape. (b) The RBCs on day 38 with predominantly discocyte shape.

Fig. 4
Fig. 4

The flow chart for automated calculation of projected surface area and mean phase of a single RBC.

Fig. 5
Fig. 5

The segmented red blood cells phase images. (a) Segmented RBCs having a stomatocyte shape, and (b) Segmented RBCs having a discocyte shape.

Fig. 6
Fig. 6

The schematic chart of different parts in the red blood cells (RBCs).

Fig. 7
Fig. 7

The segmented phase images of the B parts (area of central pallor) [see Fig. 6] in RBCs. (a) Segmented phase image of the B part in the RBCs having a stomatocyte shape. (b) Segmented phase image of the B part in the RBCs having a discocyte shape.

Fig. 8
Fig. 8

(a) Two statistical distributions for the cell area in part A [see Fig. 6] of RBCs. (b) Two statistical distributions of the mean of phase value in part A of RBCs. Solid line is for the RBCs having a stomatocyte shape. Dotted line is for the RBCs having a discocyte shape.

Fig. 9
Fig. 9

A scatter plot of the relationship between the projected surface area and the mean of the phase value in (a) A part and (b) B part [see Fig. 6] of a single RBC.

Fig. 10
Fig. 10

(a) Statistical distributions of the MCH in the A part of RBCs. (b) A scatter plot of the relationship between the MCH and MCH surface density in the A part of a single RBC.

Fig. 11
Fig. 11

Statistical distribution of the sphericity coefficient, k in A part of RBCs. Solid line is for RBCs having a stomatocyte. Dotted line is for RBCs having a discocyte shape.

Equations (6)

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S=N p 2 M 2 , φ ¯ = 1 N i=1 N x i ,
k= p h c p h d ,
DryMass(DM)= 10λ 2πα S φds = 10λ 2πα φ ¯ S,
MCHSD= MCH S .
LR=1/ [ 1+c (E[ X r ]E[ X i ] ) S pl 1 (E[ X r ]E[ X i ]) ( N r + N i 2) ] ( N r + N i ) 2 = [ 1 1+ T 2 /( N r + N i 2) ] ( N r + N i ) 2 ,
d( x ¯ , y ¯ )= i=1 n ( x ¯ i y ¯ i ) 2 ,

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